Gut Microbiota Features Associated With Campylobacter Burden and Postnatal Linear Growth Deficits in a Peruvian Birth Cohort

Rouhani, Saba; Griffin, Nicholas W.; Yori, Pablo Peñataro; Olórtegui, Maribel Paredes; Salas, Mery Siguas; Trigoso, Dixner Rengifo; Moulton, Lawrence H.; Houpt, Eric R.; Barratt, Michael J.; Kosek, Margaret; Gordon, Jeffrey I.

doi:10.1093/cid/ciz906

Cited by 30 publications

(37 citation statements)

References 48 publications

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“…Moreover, multiple species of both Haemophilus and Campylobacter cause human disease. Both Haemophilus and Campylobacter are more abundant in stunted children of the larger Afribiota population [12], and Campylobacter has been strongly and consistently associated with linear growth faltering in children [12,34,35], suggesting an important relationship with undernutrition. Both Haemophilus and Campylobacter are additionally associated with host inflammation, including the species H. parainfluenzae to which the ASV observed here was most closely related [34,36,37].…”

Section: Discussionmentioning

confidence: 99%

Immunoglobulin recognition of fecal bacteria in stunted and non-stunted children: findings from the Afribiota study

et al. 2020

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Background: Child undernutrition is a global health issue that is associated with poor sanitation and an altered intestinal microbiota. Immunoglobulin (Ig) A mediates host-microbial homeostasis in the intestine, and acutely undernourished children have been shown to have altered IgA recognition of the fecal microbiota. We sought to determine whether chronic undernutrition (stunting) or intestinal inflammation were associated with antibody recognition of the microbiota using two geographically distinct populations from the Afribiota project. Fecal bacteria from 200 children between 2 and 5 years old in Antananarivo, Madagascar, and Bangui, Central African Republic (CAR), were sorted into IgA-positive (IgA+) and IgA-negative (IgA−) populations by flow cytometry and subsequently characterized by 16S rRNA gene sequencing to determine IgA-bacterial targeting. We additionally measured IgG+ fecal bacteria by flow cytometry in a subset of 75 children. Results: Stunted children (height-forage z-score ≤ −2) had a greater proportion of IgA+ bacteria in the fecal microbiota compared to non-stunted controls. This trend was consistent in both countries, despite the higher overall IgA-targeting of the microbiota in Madagascar, but lost significance in each country individually. Two of the most highly IgA-recognized bacteria regardless of nutritional status were Campylobacter (in CAR) and Haemophilus (in both countries), both of which were previously shown to be more abundant in stunted children; however, there was no association between IgA-targeting of these bacteria and either stunting or inflammatory markers. IgGbound intestinal bacteria were rare in both stunted and non-stunted children, similar to levels observed in healthy populations.

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Section: Discussionmentioning

confidence: 99%

Immunoglobulin recognition of fecal bacteria in stunted and non-stunted children: findings from the Afribiota study

et al. 2020

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“…The effects of Giardia on gut microbiota may also be age dependent. The MAL-ED study of Peruvian children found that gut microbiota associated with Giardia burden varied by age ( 35 ). For example, high Giardia burden was associated with enrichment of Prevotella only in fecal samples of 24-month-old children.…”

Section: Discussionmentioning

confidence: 99%

“…Similarly, The Etiology, Risk Factors, and Interactions of Enteric Infections and Malnutrition and the Consequences for Child Health (MAL-ED) study investigated the hypothesis that infection with enteric pathogens contributes to undernutrition in children ( 34 ). A follow-up to the MAL-ED study performed 16S sequencing on nearly 1,000 fecal samples from participants in the Peruvian cohort to assess the taxa associated with the burden of Campylobacter and other enteric pathogens ( 35 ). We used a database mining approach to determine whether Giardia infection perturbs the human gut microbiome, in both the GEMS and MAL-ED cohorts, similarly to how it perturbs the canine gut microbiome, and to gain insight into possible mechanisms by which Giardia infection may be linked to protection against diarrhea in some individuals.…”

Section: Introductionmentioning

confidence: 99%

Natural Infection with Giardia Is Associated with Altered Community Structure of the Human and Canine Gut Microbiome

Berry

Johnson

Martins

et al. 2020

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Enteric parasitic infections are among the most prevalent infections in lower- and middle-income countries (LMICs) and have a profound impact on global public health. While the microbiome is increasingly recognized as a key determinant of gut health and human development, the impact of naturally acquired parasite infections on microbial community structure in the gut, and the extent to which parasite-induced changes in the microbiome may contribute to gastrointestinal symptoms, is poorly understood. Enteric parasites are routinely identified in companion animals in the United States, presenting a unique opportunity to leverage this animal model to investigate the impact of naturally acquired parasite infections on the microbiome. Clinical, parasitological, and microbiome profiling of a cohort of 258 dogs revealed a significant correlation between parasite infection and composition of the bacterial community in the gut. Relative to other enteric parasites, Giardia was associated with a more pronounced perturbation of the microbiome. To compare our findings to large-scale epidemiological studies of enteric diseases in humans, a database mining approach was employed to integrate clinical and microbiome data. Substantial and consistent alterations to microbiome structure were observed in Giardia-infected children. Importantly, infection was associated with a reduction in the relative abundance of potential pathobionts, including Gammaproteobacteria, and an increase in Prevotella—a profile often associated with gut health. Taken together, these data show that widespread Giardia infection in young animals and humans is associated with significant remodeling of the gut microbiome and provide a possible explanation for the high prevalence of asymptomatic Giardia infections observed across host species. IMPORTANCE While enteric parasitic infections are among the most important infections in lower- and middle-income countries, their impact on gut microbiota is poorly understood. We reasoned that clinical symptoms associated with these infections may be influenced by alterations of the microbiome that occur during infection. To explore this notion, we took a two-pronged approach. First, we studied a cohort of dogs naturally infected with various enteric parasites and found a strong association between parasite infection and altered gut microbiota composition. Giardia, one of the most prevalent parasite infections globally, had a particularly large impact on the microbiome. Second, we took a database-driven strategy to integrate microbiome data with clinical data from large human field studies and found that Giardia infection is also associated with marked alteration of the gut microbiome of children, suggesting a possible explanation for why Giardia has been reported to be associated with protection from moderate to severe diarrhea.

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“…Nevertheless, methods based on the mechanism of competitive exclusion have been widely explored, and several studies demonstrate that modification of intestinal microbiota may be effective in outcompeting Campylobacter challenges [ 10 , 11 ]. For the development of effective intervention strategies in this direction, it is important to adequately characterize the intestinal microbiota of chickens [ 12 , 13 , 14 , 15 ]. Most of the studies that have been published to date have been based on culture methods, or on relatively simplified molecular biology-based approaches [ 16 ].…”

Section: Introductionmentioning

confidence: 99%

The Interplay between Campylobacter and the Caecal Microbial Community of Commercial Broiler Chickens over Time

et al. 2021

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Campylobacter is the most frequent foodborne zoonotic bacteria worldwide, with chicken meat being overwhelmingly the most important reservoir for human infections. Control measures implemented at the farm level (i.e., biosecurity or vaccination), which have been successfully applied to limit other pathogens, such as Salmonella, have not been effective in reducing Campylobacter occurrence. Thus, new approaches are needed to fully understand the ecological interactions of Campylobacter with host animals to effectively comprehend its epidemiology. The objective of this study was to analyse longitudinally the gut microbiota composition of Campylobacter-infected and non-infected farms to identify any difference that could potentially be indicative of gut colonization by Campylobacter spp. Differences in the colonization rate and timing were observed at the farms that became positive for Campylobacter jejuni over the investigated time points, even though in positive tests, the occurrence of Campylobacter jejuni gut colonization was not observed before the second week of the life of the birds. Significant differences were observed in the abundances of specific bacterial taxa between the microbiota of individuals belonging to farms that became Campylobacter positive during the study and those who remained negative with particular reference to Bacteroidales and Clostridiales, respectively. Moreover, Campylobacter colonization dramatically influenced the microbiota richness, although to a different extent depending on the infection timing. Finally, a key role of Faecalibacterium and Lactobacillus genera on the Campylobacter microbial network was observed. Understanding the ecology of the Campylobacter interaction with host microbiota during infection could support novel approaches for broiler microbial barrier restoration. Therefore, evidence obtained through this study can be used to identify options to reduce the incidence of infection at a primary production level based on the targeted influence of the intestinal microbiota, thus helping develop new control strategies in order to mitigate the risk of human exposure to Campylobacter by chicken meat consumption.

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Gut Microbiota Features Associated With Campylobacter Burden and Postnatal Linear Growth Deficits in a Peruvian Birth Cohort

Cited by 30 publications

References 48 publications

Immunoglobulin recognition of fecal bacteria in stunted and non-stunted children: findings from the Afribiota study

Immunoglobulin recognition of fecal bacteria in stunted and non-stunted children: findings from the Afribiota study

Natural Infection with Giardia Is Associated with Altered Community Structure of the Human and Canine Gut Microbiome

The Interplay between Campylobacter and the Caecal Microbial Community of Commercial Broiler Chickens over Time

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